The nucleus accumbens and Pavlovian reward learning

Abstract

The ability to form associations between predictive environmental events and rewarding outcomes is a fundamental aspect of learned behavior. This apparently simple ability likely requires complex neural processing evolved to identify, seek, and use natural rewards and redirect these activities based on updated sensory information. Emerging evidence from both animal and human research suggests that this type of processing is mediated in part by the nucleus accumbens (NAc) and a closely associated network of brain structures. The NAc is required for a number of reward-related behaviors and processes specific information about reward availability, value, and context. In addition, this structure is critical for the acquisition and expression of most Pavlovian stimulus-reward relationships, and cues that predict rewards produce robust changes in neural activity in the NAc. Although processing within the NAc may enable or promote Pavlovian reward learning in natural situations, it has also been implicated in aspects of human drug addiction, including the ability of drug-paired cues to control behavior. This article provides a critical review of the existing animal and human literature concerning the role of the NAc in Pavlovian learning with nondrug rewards and considers some clinical ture concerning the role of the NAc in Pavlovian learning with nondrug implications of these findings.

Figure 1

General overview of key nucleus accumbens afferent and efferent projections. See text for more information on the anatomic organization of the nucleus accumbens. Note that placement of arrows does not necessarily indicate degree or precise location of projection. PFC, prefrontal cortex; HPC, hippocampus; BLA, basolateral amygdala; VTA, ventral tegmental area; VP, ventral pallidum; NAc, nucleus accumbens.

Figure 2

A single NAc neuron showing opposite firing patterns during intraoral infusion of rewarding sucrose (left) versus bitter, aversive quinine (right). After an initial excitatory response, the same NAc neuron displayed an inhibition in firing rate during sucrose infusion and an excitation in activity during quinine delivery. The onset of opposite discharge patterns (at approximately 1 s following pump onset) corresponded to the activation of EMG activity of the anterior digastric muscle indicative of licking the tastant (not shown). Intraoral infusions are denoted by the black horizontal line; data are aligned to the onset of the infusion pump (0 s). Figure taken with permission from Roitman and others, Neuron, 45: 587–597, 2005.

Figure 3

A single NAc neuron showing a characteristic increase in firing rate within seconds of the cue (lever extension) paired with sucrose (indicated by blue line under top PEH) but not the unpaired cue (extension of second lever never paired with sucrose delivery, indicated by red line under bottom PEH). A. Raster plot and PEH in a 30-s window relative to onset of the cue paired with sucrose delivery (first dashed line) and lever retraction/sucrose delivery (second dashed line). B. Raster plot and PEH for the same neuron during a 30 s window surrounding the onset of the unpaired cue. Figure modified with permission from European Journal of Neuroscience, 23, 1341–1351 (2006).

Figure 4

Rapid dopamine release in the core of the NAc, as measured with fast scan cyclic voltammetry, is observed during presentation of an audiovisual CS associated with cocaine infusion during self-administration sessions. Top, dopamine concentration significantly increased relative to CS (tone houselight) onset at time 0 in animals well-trained to self-administer the drug. Bottom, the same tone houselight stimulus did not evoke dopamine release in animals without a history of cocaine self-administration. Dopamine concentration changes are presented as means (solid line) and standard deviation of the mean (dashed line). Duration of tone houselight CS is indicated by blue line (20 s total). Figure from Nature (Phillips and others, 2003, 422:614–618).